Lessons learned from the genome analysis of Ralstonia solanacearum

Annual Review of Phytopathology

Volumn 42, Issue , 2004, Pages 107-134

  Genin, Stéphane ^a   Boucher, Christian ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

Bacterial wilt; Lateral gene transfer; Pathogenicity; Protein secretion systems; Soil bacterium

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL; EVOLUTION; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; RALSTONIA SOLANACEARUM; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; EVOLUTION; MOLECULAR SEQUENCE DATA; PLANT DISEASES; RALSTONIA SOLANACEARUM; SOIL MICROBIOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); PROKARYOTA; RALSTONIA; RALSTONIA SOLANACEARUM;

EID: 4744374965     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.phyto.42.011204.104301     Document Type: Review

References (90)

1. Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22:60-69
2. Aldon D, Brito B, Boucher B, Genin S. 2000. A bacterial sensor of plant cell contact controls the transcriptional induction oiRalstonia solanacearum pathogenicity genes. EMBOJ. 19:2304-14
3. Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T, et al. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type HI secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA 97:4856-61
4. Arnold DL, Pitman A, Jackson RW. 2003. Pathogenicity and other genomic islands in plant pathogenic bacteria. Mol. Plant Pathol. 4:407-20
5. Ball G, Durand E, Lazdunski A, Filloux A. 2002. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43:475-85
6. Basim H, Stall RE, Minsavage GV, Jones JB. 1999. Chromosomal gene transfer by conjugation in the plant pathogen Xanthomonas axonopodis pv. vesicatoria. Phytopathology 89:1044-49
7. Bertolla F, Van Gijsegem F, Nesme X, Simonet P. 1997. Conditions for natural transformation of Ralstonia solanacearum. Appl. Environ. Microbiol. 63:4965-68
8. Binet R, Letoffe S, Ghigo JM, Delepelaire P, Wandersman C. 1997. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene. 192:7-11
9. Boucher CA, Barberis P, Trigalet AP, Demery DA. 1985. Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J. Gen. Microbiol. 131:2449-57
10. Boucher C, Martinel A, Barberis P, Alloing G, Zischek C. 1986. Virulence genes are carried by a megaplasmid of the plant pathogen Pseudomonas solanacearum. Mol. Gen. Genet. 205:27075
11. Bretz JR, Mock NM, Charity JC, Zeyad S, Baker CJ, et al. 2003. A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol. Microbiol. 49:389-400
12. Brito B, Aldon D, Barberis P, Boucher C, Genin S. 2002. A signal transfer system through three compartments transduces the plant cell contact-dependent signal controlling Ralstonia solanacearum hrp genes. Mol. Plant Microbe Interact. 15:109-19
13. Burrus V, Pavlovic G, Decaris B, Guedon G. 2002. Conjugative transposons: the tip of the iceberg. Mol. Microbiol. 46:601-10
14. Buttner D, Bonas U. 2002. Getting across - bacterial type III effector proteins on their way to the plant cell. EMBO J. 21:5313-22
15. Carney BF, Denny TP. 1990. A cloned avirulence gene from Pseudomonas solanacearum determines incompatibility on Nicotiana tabacum at the host species level. J. Bacteriol. 172:4836-43
16. Casper-Lindley C, Dahlbeck D, Clark ET, Staskawicz BJ. 2002. Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci. USA. 99:8336-41
17. Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G et al. 2003. Legume symbiotic nitrogen fixation by beta-Proteobacteria is widespread in nature. J. Bacteriol. 185:7266-72
18. Coenye T, Vandamme P. 2003. Simple sequence repeats and compositional bias in the bipartite Ralstonia solanacearum GMI1000 genome. BMC Genomics 4:10
19. Coenye T, Vandamme P, LiPuma JJ. 2003. Ralstonia respiraculi sp. nov., isolated from the respiratory tract of cystic fibrosis patients. Int. J. Syst. Evol. Microbiol. 53:1339-42
20. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR. 2002. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-69
21. Cornelis GR, Van Gijsegem F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-74
22. Cunnac S, Boucher C, Genin S. 2004. Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the Type III secretion system and effector genes in Ralstonia solanacearum. J. Bacteriol. 186:2309-18
23. Cunnac S, Occhialini A, Barberis P, Boucher C, Genin S. 2004. Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the Type III secretion system. Mol. Microbiol. In press
24. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, et al. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-63
25. Deslandes L, Olivier J, Peelers N, Feng DX, Khounlotham M, et al. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. USA 100:8024-29
26. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX et al. 2002. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. USA 99:2404-9
27. De Vrind J, De Groot A, Brouwers GJ, Tommassen J, De Vrind-De long E. 2003. Identification of a novel Gsp-related pathway required for secretion of the manganese-oxidizing factor of Pseudomonas putida strain GB-1. Mol. Microbiol. 47:993-1006
28. Ding Z, Atmakuri K, Christie PJ. 2003. The outs and ins of bacterial type IV secretion substrates. Trends Microbiol. 11:527-35
29. Duetz WA, Bouwmeester H, van Beilen JB, Witholt B. 2003. Biotransformation of limonene by bacteria, fungi, yeasts, and plants. Appl. Microbiol. Biotechnol. 61:269-77
30. Durand E, Bernadac A, Ball G, Lazdunski A, Sturgis JN, et al. 2003. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185:2749-58
31. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5:199-206
32. Espinosa A, Guo M, Tam VC, Fu ZQ, Alfano JR. 2003. The Pseudomonas syringae type III-secreted protein Hop-PtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49:377-8
33. Ravier AB, Clough SJ, Schell MA, Denny TP. 1997. Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26:251-59
34. Genin S, Boucher C. 2002. Ralstonia solanacearum: secrets of a major pathogen unveiled by analysis of its genome. Mol. Plant Pathol. 3:111-18
35. Gonzalez ET, Allen C. 2003. Characterization of a Ralstonia solanacearum operon required for polygalacturonate degradation and uptake of galacturonic acid. Mol. Plant Microbe Interact. 16:536-44
36. Gophna U, Ron EZ, Graur D. 2003. Bacterial type UJ secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151-63
37. Hacker J, Carniel E. 2001. Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep. 2:376-81
38. Hacker J, Kaper JB. 2000. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:641-79
39. Hauck P, Thilmony R, He SY. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100:8577-82
40. Hayward AC. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87
41. Henderson IR, Nataro JP. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69:1231-43
42. Jacob-Dubuisson F, Locht C, Antoine R. 2001. Two-partner secretion in Gramnegative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40:306-13
43. Kanda A, Yasukohchi M, Ohnishi K, Kiba A, Okuno T, et al. 2003. Ectopic expression of Ralstonia solanacearum effector protein PopA early in invasion results in loss of virulence. Mol. Plant Microbe Interact. 16:447-55
44. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, et al. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7:331-38
45. Kang Y, Huang J, Mao G, He LY, Schell MA. 1994. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol. Plant Microbe Interact. 7:370-77
46. Kang Y, Liu H, Genin S, Schell MA, Denny TP. 2002. Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol. Microbiol. 46:427-37
47. Kim JG, Park BK, Yoo CH, Jeon E, Oh J, et al. 2003. Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J. Bacterial. 185:3155-66
48. Lavie M, Seunes B, Prior P, Boucher C. 2004. Distribution of a family of type III dependent effectors correlates with the phylogeny of Ralstonia solanacearum strains. Mol. Plant Microbe Interact. In press
49. Lavie M; Shillington E, Eguiluz C, Grimsley N, Boucher C. 2002. PopP1, a new member of the YopJ/AvrRxv family of type III effector proteins, acts as a host-specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol. Plant Microbe Interact. 15:1058-68
50. Lawrence JG, Roth JR. 1996. Selfish operons: Horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843-60
51. Liu H, Kang Y, Genin S, Schell MA, Denny TP. 2001. Twitching motility of Ralstonia solanacearum requires a type IV pilus system. Microbiology 147:3215-29
52. Martin P, van de Yen T, Mouchel N, Jeffries AC, Hood DW, et al. 2003. Experimentally revised repertoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. Mol. Microbiol. 50:245-57
53. Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, et al. 2003. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol. Rev. 27:385-410
54. Metzgar D, Wills C. 2000. Evolutionary changes in mutation rates and spectra and their influence on the adaptation of pathogens. Microbes Infect. 2:1513-22
55. Morales VM, Sequeira L. 1985. Indigenous plasmids in Pseudomonas solanacearum. Phytopathology 60:833-38
56. Moxon ER, Rainey PB, Nowak MA, Lenski RE. 1994. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4:24-33
57. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, et al. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4:799-808
58. Nies DH. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27:313-39
59. Noel L, Thieme F, Nennstiel D, Bonas U. 2002. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol. 184:1340-48
60. Nurnberger T, Brunner F. 2002. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5:318-24
61. Ochman H, Moran NA. 2001. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096-99
62. Ojanen-Reuhs T, Kalkkinen N, Westerlund-Wikstrom B, van Doom J, Haahtela K, et al. 1997. Characterization of the fimA gene encoding bundle-forming fimbriae of the plant pathogen Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 179:1280-90
63. Planet PJ, Kachlany SC, Fine DH, DeSalle R, Figurski DH. 2003. The widespread colonization island of Actinobacillus actinomycetemcomitans. Nat. Genet. 34:193-98
64. Poussier S, Thoquet P, Trigalet-Demery D, Barthet S, Meyer D, et al. 2003. Host plant-dependent phenotypic reversion of Ralstonia solanacearum from non-pathogenic to pathogenic forms via alterations in the phcA gene. Mol. Microbiol. 49:991-1003
65. Rainbow L, Hart CA, Winstanley C. 2002. Distribution of type III secretion gene clusters in Burkholderia pseudomallei, B. thailandensis and B. mallei. J. Med. Microbiol. 51:374-84
66. Ray SK, Rajeshwari R, Sharma Y, Sonti RV. 2002. A high-molecular-weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence. Mol. Microbiol. 46:637-47
67. Roine E, Raineri DM, Romantschuk M, Wilson M, Nunn DN. 1998. Characterization of type FV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant Microbe Interact. 11:1048-56
68. Rojas CM, Ham JH, Deng WL, Doyle JJ, Collmer A. 2002. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC 16 on Nicotiana clevelandii seedlings. Proc. Natl. Acad. Sci. USA 99:13142-47
69. Rosenberg C, Casse-Delbart F, Dusha I, David M, Boucher C. 1982. Megaplasmids in the plant-associated bacteria Rhizobium meliloti and Pseudomonas solanacearum. J. Bacterial. 150:402-6
70. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, et al. 2002. Genome sequence of the plant pathogen Ralsionia solanacearum. Nature 415:497-502
71. Sandkvist M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271-83
72. Schell MA. 2000. Regulation of virulence and pathogenicity genes in Ralstonia solanacearum by a complex network. Annu. Rev. Phytopathol. 38:263-92
73. Seo S, Seto H, Koshino H, Yoshida S, Ohashi Y. 2003. A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco. Plant Cell 15:863-73
74. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-88
75. Sory MP, Cornelis GR. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-94
76. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-64
77. Sudakevitz D, Imberty A, Gilboa-Garber N. 2002. Production, properties and specificity of a new bacterial L-fucose- and D-arabinose-binding lectin of the plant pathogen Ralstonia solanacearum, and its comparison to related plant and microbial lectins. J. Biochem. 132:353-58
78. Sudakevitz D, Kostlanova N, Blatman-Jan G, Mitchell EP, Lerrer B, et al. 2004. A new Ralstonia solanacearum high affinity mannose-binding lectin RS-IIL structurally resembling the Pseudomonas aeruginosa fucose-specific lectin PA-IIL. Mol. Microbiol. In press
79. Szurek B, Marois E, Bonas U, Van den Ackerveken G. 2001. Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26:523-34
80. Tans-Kersten J, Huang H, Allen C. 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacterial. 183:3597-605
81. Toussaint A, Merlin C, Monchy S, Benotmane MA, Leplae R, et al. 2003. The biphenyl- and 4-chlorobiphenyl-catabolic transposon Tn4371, a member of a new family of genomic islands related to IncP and Ti plasmids. Appl. Environ. Microbiol. 69:4837-15
82. Trigalet A, Demery D. 1986. Invasiveness in tomato plants of Tn5-induced mutants of Pseudomonas solanacearum. Physiol. Mol. Plant Pathol. 28:423-30
83. Tsiamis G, Mansfield JW, Hockenhull R, Jackson RW, Sesma A, et al. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19:3204-14
84. Van Gijsegem F, Gough C, Zischek C, Niqueux E, Arlat M, et al. 1995. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15:1095-114
85. 82a. Van Sluys MA, Monteiro-Vitorello CB, Camargo LE, Menck CF, Da Silva AC, et al. 2002. Comparative genomic analysis of plant-associated bacteria. Annu. Rev. Phytopathol. 40:169-89
86. Vasse J, Genin S, Frey P, Boucher C, Brito B. 2000. The hrpB and hrpG regulatory genes of Ralstonia solanacearum are required for different stages of the tomato root infection process. Mol. Plant Microbe Interact. 13:259-67
87. Versees W, Decanniere K, Pelle R, Depoorter J, Brosens E, et al. 2001. Structure and function of a novel purine specific nucleoside hydrolase from Trypanosoma vivax. J. Mol. Biol. 307:1363-79
88. White FF, Yang B, Johnson LB. 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3:291-98
89. Young BM, Young GM. 2002. Yp1A is exported by the Ysc, Ysa, and flagellar type III secretion systems of Yersinia enterocolitica. J. Bacteriol. 184:1324-34
90. Zhu W, Yang B, Wills N, Johnson LB, White FF. 1999. The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell 11:1665-74